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Interpretive Summary: Ticks transmit bacterial pathogens throughout all continents and are one of the primary vectors of zoonotic diseases. With more than 15 new tick-borne bacterial pathogens discovered since the discovery of Lyme disease in 1981, ticks are harbingers of emerging diseases. Dermacentor andersoni, the Rocky Mountain wood tick, can transmit several human pathogens, including Rickettsia rickettsii, Colorado tick fever virus, and Francisella tularensis. It is also a vector of Anaplasma marginale, the most widespread tick-borne pathogen of livestock worldwide, which has significant implications for food security in the developing world. A prominent knowledge gap in understanding tick-pathogen biology is how the bacterial microbiome of the tick interacts with pathogens. Although the microbiome of D. andersoni is previously unexplored, targeted studies suggest that rickettsial species have a negative correlation on one another. Our study characterizes the bacterial microbiome of D. andersoni and provides evidence of rickettsial interference between a rickettsial endosymbiont and A. marginale. In addition, we demonstrate that a high proportion of Francisella endosymbionts in the tick microbiome results in higher F. novicida infection levels.

Technical Abstract: Ticks are of medical and veterinary importance due to their ability to transmit pathogens to humans and animals. The Rocky Mountain wood tick, Dermacentor andersoni, is a vector of a number of pathogens, including Anaplasma marginale, which is the most widespread tick-borne pathogen of livestock. Although ticks host pathogenic bacteria, they also harbor bacterial endosymbionts that play a role in tick physiology, survival, as well as pathogen acquisition and transmission. The goal of this study was to characterize the bacterial microbiome and examine the impact of microbiome disruption on pathogen susceptibility. The bacterial microbiome of two populations of D. andersoni with historically different susceptibilities to A. marginale was characterized. In this study, the microbiome was disrupted and then ticks were exposed to A. marginale or Francisella novicida to determine if the microbiome correlated with pathogen susceptibility. Our study showed that an increase in proportion and quantity of Ricketttsia bellii in the microbiome was negatively correlated to A. marginale levels in ticks. Furthermore, a decrease in Francisella endosymbionts was associated with lower F. novicida levels, demonstrating a positive pathogen-endosymbiont relationship. We demonstrate that endosymbionts and pathogens have varying interactions, and suggest that microbiome manipulation can provide a possible method for biocontrol by decreasing pathogen susceptibility of ticks.